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Created: 09 Sep 2015

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Volume 6, October 2016

Newsletter

3D at Purdue

3D in Focus

3D in Publications

3D in Meetings

3D at Purdue

New Thermogels for Culturing Cells in 3D Structures

Kinam Park and Bumsoo Han

Culturing cells in 3D structures provides many advantages over 2D models. Cells in 3D structures often behave differently from those in 2D cultures. For example, cancer cells organized in 3D spheroids are often more resistant to anticancer drugs than cells in 2D cultures. Several types of commercially available products allow researchers to produce multicellular spheroids. The products are classified into (i) extracellular matrices based on cellular extracts, (ii) natural polymers, and (iii) cell culture plates with non-cell adherent surface or with no surface for the cells to attach. Each method has its own advantages and limitations.

Recently, we developed simple polymeric systems that allow cells to form 3D structures. The polymers are named “3DCellMaker” for its ability to culture various types of cells and cell mixtures in 3D (Fig. 1). 3DCellMakers are inverse themosensitive gels (thermogels), i.e., they remain in liquid form at room temperature or lower and become a gel at 37 °C. These thermogels are poloxamers-poly(ester-urethane) copolymers or stearate-modified methyl cellulose. For the culture process, the cells can be placed on top of the formed gels, or they can be mixed with the thermogels at low temperature before incubating at 37 °C. The simplicity, and low cost, of using 3DCellMaker allows culturing of various cell types in 3D for high throughput screening. The synthetic nature of the 3DCellMaker makes it easy to control the gel’s properties. The 3DCellMaker also allows culture of cells with defined additives, under serum-free conditions (Fig. 2). 3DCellMaker thermogels are available for free for researchers at Purdue University.

Fig. 1. Co-culture of MCF-7 breast cancer cells and CCD-1068SK fibroblasts in a 3DCellMaker for five days. (Scale bar is 100 mm).

Fig. 2 Culture of T4-2 breast cancer cells after two days in a 3DCellMaker under a serum-free condition (20X objective; courtey picture from the Lelièvre laboratory).

3D in Focus

Angiogenesis is the process for new blood vessel formation through sprouting of endothelial cells from existing vessels. This process is regulated by biochemical and mechanical pathways. However, the effects of mechanical stimuli remain poorly appreciated and understood. Recent studies using microfabricated 3D culture systems have highlighted critical roles for flow-induced mechanical stimuli in angiogenesis. In this newsletter we are highlighting the work of Kim and colleagues on the role of mechanical stimuli in angiogenic sprouting using microfluidics.

Sudong Kim, Minhwan Chung, Jungho Ahn, Somin Leeb and Noo Li Jeon “Interstitial flow regulates the angiogenic response and phenotype of endothelial cells in a 3D culture model” Lab Chip, 2016, 16, 4189 - 4199

The authors have designed a microfluidic system with six parallel microchannels for the investigation of individual or combined effects of biochemical and mechanical factors during the initiation and outgrowth of angiogenic sprouts within the extracellular matrix. One of the two central channels is loaded with a fibrin matrix in which endothelial cells (ECs) are embedded (channel N); the other central channel contains an acellular fibrin matrix (channel S). The two outermost channels are used for the culture of stromal fibroblasts in the presence of fibrin. Fluidic channels located in-between the central and outermost channels are filled with culture medium with a flow at physiological level 0.1 – 4 μm S^-1. The intent is for the soluble proangiogenic factors secreted by the fibroblasts to act on the ECs via the fluidic channels.

The initial phase of angiogenesis includes angiogenic sprout, vacuole formation within endothelial cells, and formation of a vascular network. Under static conditions in the device, angiogenic sprout extended from the cytoplasm of ECs (channel N), and these cells initiated vacuole formation that progressively developed into complex vascular networks. The sprouts extended first near the interface of channels N and S, and further into adjacent channel S where the ECs organized multicellular structures characterized by abundant actin-rich filopodia at their edges distal from the N channels thus, morphologically replicating the sprout tip of endothelial cells in vivo.

Moreover, the interstitial flow in the S to N direction in the fluidic channels promoted the formation of sprouts with a significantly greater number of filopodia projections compared to those formed under static conditions. In contrast, interstitial flow in the N to S direction completely inhibited the angiogenic sprouting. Unlike angiogenic sprouts, vacuole formation and the development of a vascular structure in channel N were not affected by the direction of the flow. Additional experiments confirmed that the interstitial flow controlled the initiation and sustained the growth of angiogenic sprouting. Reversing the direction of the interstitial flow to S-N abolished the suppressor effect of N-S flow on sprouting. On the other hand, reversing the flow direction from S-N to N-S had no effect on the existing vascular structure, but it induced less filopodia projections and the retraction of the forefront of the vasculature.

The model was subsequently examined for its capability to evaluate endothelial responses (i.e., sprout initiation, formation of vacuoles, vascular network formation) to extrinsic proangiogenic factors, such as VEGF, as well as anti-angiogenic compounds such as axitinib.

Angiogenesis is fundamental to many physiologic and pathologic processes such as cancer, ischemic diseases, and chronic inflammation. By acting as a proangiogenic stimulant, the interstitial flow in blood vessels can modulate the endothelial responses triggered by the biochemical stimuli such as VEGF. The authors propose that the device can help elucidate the relevant mechanisms and thus, may lead to the development of effective therapeutics for diseases associated with angiogenesis.

The model designed here is interesting because of the addition of fibroblasts compared to the usual stand-alone endothelial cells to study angiogenesis within a microfluidics platform. The fibroblasts provide the angiogenic factors, making the model more physiologically relevant.

3D in Publications

Complete List -- 3D culture related articles on PubMed (last 2 months)

Reviews

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3D in Publications

Complete List

Abbadessa, A., Blokzijl, M. M., Mouser, V. H., Marica, P., Malda, J., Hennink, W. E., and Vermonden, T. (2016). A thermo-responsive and photo-polymerizable chondroitin sulfate-based hydrogel for 3D printing applications. Carbohydr Polym 149, 163-174.

Adams, C. F., Dickson, A. W., Kuiper, J. H., and Chari, D. M. (2016). Nanoengineering neural stem cells on biomimetic substrates using magnetofection technology. Nanoscale 8, 17869-17880.

Aihara, A., Abe, N., Saruhashi, K., Kanaki, T., and Nishino, T. (2016). A Novel 3-D Cell Culture System for In Vitro Evaluation of Anticancer Drugs under Anchorage-Independent Conditions. Cancer Sci.

Akasov, R., Gileva, A., Zaytseva-Zotova, D., Burov, S., Chevalot, I., Guedon, E., and Markvicheva, E. (2016). 3D in vitro co-culture models based on normal cells and tumor spheroids formed by cyclic RGD-peptide induced cell self-assembly. Biotechnol Lett.

Alborzinia, H., Shaikhkarami, M., Hortschansky, P., and Wolfl, S. (2016). BMP2 Transfer to Neighboring Cells and Activation of Signaling. Traffic 17, 1042-1053.

Alexander, P. G., Clark, K. L., and Tuan, R. S. (2016). Prenatal exposure to environmental factors and congenital limb defects. Birth Defects Res C Embryo Today.

Allen, E. L., Ulanet, D. B., Pirman, D., Mahoney, C. E., Coco, J., Si, Y., Chen, Y., Huang, L., Ren, J., Choe, S., et al. (2016). Differential Aspartate Usage Identifies a Subset of Cancer Cells Particularly Dependent on OGDH. Cell Rep 17, 876-890.

Amaral, A. J., and Pasparakis, G. (2016). Rapid Formation of Cell Aggregates and Spheroids Induced by a "Smart" Boronic Acid Copolymer. ACS Appl Mater Interfaces 8, 22930-22941.

Arai, K., Eguchi, T., Rahman, M. M., Sakamoto, R., Masuda, N., Nakatsura, T., Calderwood, S. K., Kozaki, K., and Itoh, M. (2016a). A Novel High-Throughput 3D Screening System for EMT Inhibitors: A Pilot Screening Discovered the EMT Inhibitory Activity of CDK2 Inhibitor SU9516. PLoS One 11, e0162394.

Arai, K., Yoshida, T., Okabe, M., Goto, M., Mir, T. A., Soko, C., Tsukamoto, Y., Akaike, T., Nikaido, T., Zhou, K., and Nakamura, M. (2016b). Fabrication of 3D-culture platform with sandwich architecture for preserving liver-specific functions of hepatocytes using 3D bioprinter. J Biomed Mater Res A.

Ardjomandi, N., Huth, J., Stamov, D. R., Henrich, A., Klein, C., Wendel, H. P., Reinert, S., and Alexander, D. (2016). Surface biofunctionalization of beta-TCP blocks using aptamer 74 for bone tissue engineering. Mater Sci Eng C Mater Biol Appl 67, 267-275.

Arevalos, C. A., Berg, J. M., Nguyen, J. M., Godfrey, E. L., Iriondo, C., and Grande-Allen, K. J. (2016). Valve Interstitial Cells Act in a Pericyte Manner Promoting Angiogensis and Invasion by Valve Endothelial Cells. Ann Biomed Eng 44, 2707-2723.

Arjmand, F., Khanmohammadi, M., Arasteh, S., Mohammadzadeh, A., Kazemnejad, S., and Akhondi, M. M. (2016). Extended Culture of Encapsulated Human Blastocysts in Alginate Hydrogel Containing Decidualized Endometrial Stromal Cells in the Presence of Melatonin. Mol Biotechnol 58, 684-694.

Arya, A. D., Hallur, P. M., Karkisaval, A. G., Gudipati, A., Rajendiran, S., Dhavale, V., Ramachandran, B., Jayaprakash, A., Gundiah, N., and Chaubey, A. (2016). Gelatin Methacrylate Hydrogels as Biomimetic Three-Dimensional Matrixes for Modeling Breast Cancer Invasion and Chemoresponse in Vitro. ACS Appl Mater Interfaces 8, 22005-22017.

Backer, A., Erhardt, O., Wietbrock, L., Schel, N., Goppert, B., Abaffy, P., Sollich, T., Cecilia, A., and Gruhl, F. J. (2016). Silk scaffolds connected with different naturally occurring biomaterials for prostate cancer cell cultivation in 3D. Biopolymers.

Bartfeld, S. (2016). Modeling infectious diseases and host-microbe interactions in gastrointestinal organoids. Dev Biol.

Belli, V., Guarnieri, D., Biondi, M., Della Sala, F., and Netti, P. A. (2016). Dynamics of nanoparticle diffusion and uptake in three-dimensional cell cultures. Colloids Surf B Biointerfaces 149, 7-15.

Bhatia, M., Lovitt, C. J., Raninga, P. V., Avery, V. M., Di Trapani, G., and Tonissen, K. F. (2016). Expression of the thioredoxin system in an in vivo-like cancer cell environment upon auranofin treatment. Eur J Cell Biol 95, 378-388.

Boehme, K. A., Nitsch, J., Riester, R., Handgretinger, R., Schleicher, S. B., Kluba, T., and Traub, F. (2016). Arsenic trioxide potentiates the effectiveness of etoposide in Ewing sarcomas. Int J Oncol.

Bono, N., Pezzoli, D., Levesque, L., Loy, C., Candiani, G., Fiore, G. B., and Mantovani, D. (2016). Unraveling the role of mechanical stimulation on smooth muscle cells: A comparative study between 2D and 3D models. Biotechnol Bioeng 113, 2254-2263.

Booij, T. H., Klop, M. J., Yan, K., Szantai-Kis, C., Szokol, B., Orfi, L., van de Water, B., Keri, G., and Price, L. S. (2016). Development of a 3D Tissue Culture-Based High-Content Screening Platform That Uses Phenotypic Profiling to Discriminate Selective Inhibitors of Receptor Tyrosine Kinases. J Biomol Screen 21, 912-922.

Borg, D. J., Welzel, P. B., Grimmer, M., Friedrichs, J., Weigelt, M., Wilhelm, C., Prewitz, M., Stissel, A., Hommel, A., Kurth, T., et al. (2016). Macroporous biohybrid cryogels for co-housing pancreatic islets with mesenchymal stromal cells. Acta Biomater 44, 178-187.

Bradley, R. S., Robinson, I. K., and Yusuf, M. (2016). 3D X-Ray Nanotomography of Cells Grown on Electrospun Scaffolds. Macromol Biosci.

Brandenberg, N., and Lutolf, M. P. (2016). In Situ Patterning of Microfluidic Networks in 3D Cell-Laden Hydrogels. Adv Mater 28, 7450-7456.

Bretschneider, H., Stiehler, M., Hartmann, A., Boger, E., Osswald, C., Mollenhauer, J., Gaissmaier, C., and Gunther, K. P. (2016). Characterization of primary chondrocytes harvested from hips with femoroacetabular impingement. Osteoarthritis Cartilage 24, 1622-1628.

Brooks, J. C., Ford, K. I., Holder, D. H., Holtan, M. D., and Easley, C. J. (2016). Macro-to-micro interfacing to microfluidic channels using 3D-printed templates: application to time-resolved secretion sampling of endocrine tissue. Analyst 141, 5714-5721.

Broutier, L., Andersson-Rolf, A., Hindley, C. J., Boj, S. F., Clevers, H., Koo, B. K., and Huch, M. (2016). Culture and establishment of self-renewing human and mouse adult liver and pancreas 3D organoids and their genetic manipulation. Nat Protoc 11, 1724-1743.

Cairns, D. M., Chwalek, K., Moore, Y. E., Kelley, M. R., Abbott, R. D., Moss, S., and Kaplan, D. L. (2016). Expandable and Rapidly Differentiating Human Induced Neural Stem Cell Lines for Multiple Tissue Engineering Applications. Stem Cell Reports 7, 557-570.

Carvalho, M. P., Costa, E. C., Miguel, S. P., and Correia, I. J. (2016). Tumor spheroid assembly on hyaluronic acid-based structures: A review. Carbohydr Polym 150, 139-148.

Celik, E., Bayram, C., Akcapinar, R., Turk, M., and Denkbas, E. B. (2016). The effect of calcium chloride concentration on alginate/Fmoc-diphenylalanine hydrogel networks. Mater Sci Eng C Mater Biol Appl 66, 221-229.

Cepeda, M. A., Pelling, J. J., Evered, C. L., Williams, K. C., Freedman, Z., Stan, I., Willson, J. A., Leong, H. S., and Damjanovski, S. (2016). Less is more: low expression of MT1-MMP is optimal to promote migration and tumourigenesis of breast cancer cells. Mol Cancer 15, 65.

Chai, Y. W., Lee, E. H., Gubbe, J. D., and Brekke, J. H. (2016). 3D Cell Culture in a Self-Assembled Nanofiber Environment. PLoS One 11, e0162853.

Chatzinikolaidou, M. (2016). Cell spheroids: the new frontiers in in vitro models for cancer drug validation. Drug Discov Today 21, 1553-1560.

Chatzinikolaidou, M., Pontikoglou, C., Terzaki, K., Kaliva, M., Kalyva, A., Papadaki, E., Vamvakaki, M., and Farsari, M. (2016). Recombinant human bone morphogenetic protein 2 (rhBMP-2) immobilized on laser-fabricated 3D scaffolds enhance osteogenesis. Colloids Surf B Biointerfaces 149, 233-242.

Chen, C., Mehl, B. T., Sell, S. A., and Martin, R. S. (2016a). Use of electrospinning and dynamic air focusing to create three-dimensional cell culture scaffolds in microfluidic devices. Analyst 141, 5311-5320.

Chen, C. S. (2016). 3D Biomimetic Cultures: The Next Platform for Cell Biology. Trends Cell Biol.

Chen, H. Y., Kaya, K. D., Dong, L., and Swaroop, A. (2016b). Three-dimensional retinal organoids from mouse pluripotent stem cells mimic in vivo development with enhanced stratification and rod photoreceptor differentiation. Mol Vis 22, 1077-1094.

Chimenti, I., Pagano, F., Angelini, F., Siciliano, C., Mangino, G., Picchio, V., De Falco, E., Peruzzi, M., Carnevale, R., Ibrahim, M., et al. (2016). Human Lung Spheroids as In Vitro Niches of Lung Progenitor Cells With Distinctive Paracrine and Plasticity Properties. Stem Cells Transl Med.

Chingwaru, W., Glashoff, R. H., Vidmar, J., Kapewangolo, P., and Sampson, S. L. (2016). Mammalian cell cultures as models for Mycobacterium tuberculosis-human immunodeficiency virus (HIV) interaction studies: A review. Asian Pac J Trop Med 9, 832-838.

Chitrangi, S., Nair, P., and Khanna, A. (2016). 3D engineered In vitrohepatospheroids for studying drug toxicity and metabolism. Toxicol In Vitro.

Choi, J., Iich, E., and Lee, J. H. (2016). Organogenesis of adult lung in a dish: Differentiation, disease and therapy. Dev Biol.

Colacino, J. A. (2016). 3D human tissue culture: modeling environmental effects on the stem cell epigenome. Epigenomics.

Colak, B., Da Silva, J. C., Soares, T. A., and Gautrot, J. E. (2016). Impact of the Molecular Environment on Thiol-Ene Coupling For Biofunctionalization and Conjugation. Bioconjug Chem 27, 2111-2123.

Connell, J. L., Ritschdorff, E. T., and Shear, J. B. (2016). 3D Printing of Photoresponsive Biomaterials for Control of Bacterial Microenvironments. Anal Chem.

Cudre-Cung, H. P., Zavadakova, P., do Vale-Pereira, S., Remacle, N., Henry, H., Ivanisevic, J., Tavel, D., Braissant, O., and Ballhausen, D. (2016). Ammonium accumulation is a primary effect of 2-methylcitrate exposure in an in vitro model for brain damage in methylmalonic aciduria. Mol Genet Metab 119, 57-67.

Dai, X., Ma, C., Lan, Q., and Xu, T. (2016). 3D bioprinted glioma stem cells for brain tumor model and applications of drug susceptibility. Biofabrication 8, 045005.

Das, P. K., Puusepp, L., Varghese, F. S., Utt, A., Ahola, T., Kananovich, D. G., Lopp, M., Merits, A., and Karelson, M. (2016). Design and validation of novel chikungunya virus protease inhibitors. Antimicrob Agents Chemother.

Deharde, D., Schneider, C., Hiller, T., Fischer, N., Kegel, V., Lubberstedt, M., Freyer, N., Hengstler, J. G., Andersson, T. B., Seehofer, D., et al. (2016). Bile canaliculi formation and biliary transport in 3D sandwich-cultured hepatocytes in dependence of the extracellular matrix composition. Arch Toxicol 90, 2497-2511.

DeJonge, R. E., Liu, X. P., Deig, C. R., Heller, S., Koehler, K. R., and Hashino, E. (2016). Modulation of Wnt Signaling Enhances Inner Ear Organoid Development in 3D Culture. PLoS One 11, e0162508.

Diermeier, S. D., Chang, K. C., Freier, S. M., Song, J., El Demerdash, O., Krasnitz, A., Rigo, F., Bennett, C. F., and Spector, D. L. (2016). Mammary Tumor-Associated RNAs Impact Tumor Cell Proliferation, Invasion, and Migration. Cell Rep 17, 261-274.

Dong, W., Lu, A., Zhao, J., Yin, S., Ou, B., and Feng, H. (2016). An efficient and simple co-culture method for isolating primary human hepatic cells: Potential application for tumor microenvironment research. Oncol Rep 36, 2126-2134.

Dubiak-Szepietowska, M., Karczmarczyk, A., Winckler, T., and Feller, K. H. (2016). A cell-based biosensor for nanomaterials cytotoxicity assessment in three dimensional cell culture. Toxicology 370, 60-69.

Eder, T., Weber, A., Neuwirt, H., Grunbacher, G., Ploner, C., Klocker, H., Sampson, N., and Eder, I. E. (2016). Cancer-Associated Fibroblasts Modify the Response of Prostate Cancer Cells to Androgen and Anti-Androgens in Three-Dimensional Spheroid Culture. Int J Mol Sci 17.

Fan, R., Piou, M., Darling, E., Cormier, D., Sun, J., and Wan, J. (2016). Bio-printing cell-laden Matrigel-agarose constructs. J Biomater Appl.

Fitzgerald, K. A., Guo, J., Raftery, R. M., Castano, I. M., Curtin, C. M., Gooding, M., Darcy, R., FJ, O. B., and CM, O. D. (2016). Nanoparticle-mediated siRNA delivery assessed in a 3D co-culture model simulating prostate cancer bone metastasis. Int J Pharm 511, 1058-1069.

Flanagan, D. J., Schwab, R. H., Tran, B. M., Phesse, T. J., and Vincan, E. (2016). Isolation and Culture of Adult Intestinal, Gastric, and Liver Organoids for Cre-recombinase-Mediated Gene Deletion. Methods Mol Biol.

Flood, P., Alvarez, L., and Reynaud, E. G. (2016). Free-floating epithelial micro-tissue arrays: a low cost and versatile technique. Biofabrication 8, 045006.

Fong, E. L., Harrington, D. A., Farach-Carson, M. C., and Yu, H. (2016). Heralding a new paradigm in 3D tumor modeling. Biomaterials 108, 197-213.

Funk, C., and Roth, A. (2016). Current limitations and future opportunities for prediction of DILI from in vitro. Arch Toxicol.

Galli, C., Parisi, L., Piergianni, M., Smerieri, A., Passeri, G., Guizzardi, S., Costa, F., Lumetti, S., Manfredi, E., and Macaluso, G. M. (2016). Improved scaffold biocompatibility through anti-Fibronectin aptamer functionalization. Acta Biomater 42, 147-156.

Galuppo, A. G., Chagastelles, P. C., Gamba, D., Iglesias, D. B., Sperling, L., Machado, J., Wendorff, J., Petzhold, C. L., and Pranke, P. (2016). Effect of feeder free poly(lactide-co-glycolide) scaffolds on morphology, proliferation and pluripotency of mouse embryonic stem cells. J Biomed Mater Res A.

Gao, Q., Wang, Z. C., Duan, M., Lin, Y. H., Zhou, X. Y., Worthley, D. L., Wang, X. Y., Niu, G., Xia, Y., Deng, M., et al. (2016). Cell Culture System for Analysis of Genetic Heterogeneity Within Hepatocellular Carcinomas and Response to Pharmacologic Agents. Gastroenterology.

Ghanavati, Z., Orazizadeh, M., Bayati, V., Abbaspour, M. R., Khorsandi, L., Mansouri, E., and Neisi, N. (2016). Characterization of A Three-Dimensional Organotypic Co-Culture Skin Model for Epidermal Differentiation of Rat Adipose-Derived Stem Cells. Cell J 18, 289-301.

Gomes, A., Guillaume, L., Grimes, D. R., Fehrenbach, J., Lobjois, V., and Ducommun, B. (2016). Oxygen Partial Pressure Is a Rate-Limiting Parameter for Cell Proliferation in 3D Spheroids Grown in Physioxic Culture Condition. PLoS One 11, e0161239.

Gomez-Leduc, T., Hervieu, M., Legendre, F., Bouyoucef, M., Gruchy, N., Poulain, L., de Vienne, C., Herlicoviez, M., Demoor, M., and Galera, P. (2016). Chondrogenic commitment of human umbilical cord blood-derived mesenchymal stem cells in collagen matrices for cartilage engineering. Sci Rep 6, 32786.

Gomez-Roman, N., Stevenson, K., Gilmour, L., Hamilton, G., and Chalmers, A. J. (2016). A novel 3D human glioblastoma cell culture system for modeling drug and radiation responses. Neuro Oncol.

Gonzalez-Valverde, I., Semino, C., and Garcia-Aznar, J. M. (2016). Phenomenological modelling and simulation of cell clusters in 3D cultures. Comput Biol Med 77, 249-260.

Gorgun, C., Ozturk, S., Gokalp, S., Vatansever, S., Gurhan, S. I., and Urkmez, A. S. (2016). Synergistic role of three dimensional niche and hypoxia on conservation of cancer stem cell phenotype. Int J Biol Macromol 90, 20-26.

Guneta, V., Tan, N. S., Chan, S. K., Tanavde, V., Lim, T. C., Wong, T. C., and Choong, C. (2016). Comparative study of adipose-derived stem cells and bone marrow-derived stem cells in similar microenvironmental conditions. Exp Cell Res.

Gurusinghe, S., Hilbert, B., Trope, G., Wang, L., Bandara, N., and Strappe, P. (2016). Generation of Immortalised Equine Chondrocytes With Inducible Sox9 Expression Allows Control of Hypertrophic Differentiation. J Cell Biochem.

Han, H. W., and Hsu, S. H. (2016). Chitosan-hyaluronan based 3D co-culture platform for studying the crosstalk of lung cancer cells and mesenchymal stem cells. Acta Biomater 42, 157-167.

Hansen, M., Met, O., Larsen, N. B., Rosenkilde, M. M., Andersen, M. H., Svane, I. M., and Hjorto, G. M. (2016). Autocrine CCL19 blocks dendritic cell migration toward weak gradients of CCL21. Cytotherapy 18, 1187-1196.

Hao, Y., Zerdoum, A. B., Stuffer, A. J., Rajasekaran, A. K., and Jia, X. (2016). Biomimetic Hydrogels Incorporating Polymeric Cell-Adhesive Peptide to Promote the 3D Assembly of Tumoroids. Biomacromolecules.

Haque, A., Gheibi, P., Gao, Y., Foster, E., Son, K. J., You, J., Stybayeva, G., Patel, D., and Revzin, A. (2016). Cell biology is different in small volumes: endogenous signals shape phenotype of primary hepatocytes cultured in microfluidic channels. Sci Rep 6, 33980.

Harris, S., Shubin, S. P., Wegner, S., Van Ness, K., Green, F., Hong, S. W., and Faustman, E. M. (2016). The presence of macrophages and inflammatory responses in an in vitro testicular co-culture model of male reproductive development enhance relevance to in vivo conditions. Toxicol In Vitro 36, 210-215.

Heidari Kani, M., Chan, E. C., Young, R. C., Butler, T., Smith, R., and Paul, J. W. (2016). 3D Cell Culturing and Possibilities for Myometrial Tissue Engineering. Ann Biomed Eng.

Hibiya, S., Tsuchiya, K., Hayashi, R., Fukushima, K., Horita, N., Watanabe, S., Shirasaki, T., Nishimura, R., Kimura, N., Nishimura, T., et al. (2016). Long-term inflammation transforms intestinal epithelial cells of colonic organoids. J Crohns Colitis.

Higuchi, Y., Kawai, K., Kanaki, T., Yamazaki, H., Chesne, C., Guguen-Guillouzo, C., and Suemizu, H. (2016). Functional polymer-dependent 3D culture accelerates the differentiation of HepaRG cells into mature hepatocytes. Hepatol Res 46, 1045-1057.

Hiler, D. J., Barabas, M. E., Griffiths, L. M., and Dyer, M. A. (2016). Reprogramming of mouse retinal neurons and standardized quantification of their differentiation in 3D retinal cultures. Nat Protoc 11, 1955-1976.

Hinton, T. J., Hudson, A., Pusch, K., Lee, A., and Feinberg, A. W. (2016). 3D Printing PDMS Elastomer in a Hydrophilic Support Bath via Freeform Reversible Embedding. ACS Biomater Sci Eng 2, 1781-1786.

Hof, A., Raschke, S., Baier, K., Nehrenheim, L., Selig, J. I., Schomaker, M., Lichtenberg, A., Meyer, H., and Akhyari, P. (2016). Challenges in developing a reseeded, tissue-engineered aortic valve prosthesis. Eur J Cardiothorac Surg 50, 446-455.

Hogrebe, N. J., and Gooch, K. J. (2016). Direct influence of culture dimensionality on human Mesenchymal stem cells differentiation at various matrix stiffnesses using a fibrous self-assembling peptide hydrogel. J Biomed Mater Res A 104, 2356-2368.

Hogrebe, N. J., Reinhardt, J. W., and Gooch, K. J. (2016). Biomaterial microarchitecture: A potent regulator of individual cell behavior and multicellular organization. J Biomed Mater Res A.

Horvath, P., Aulner, N., Bickle, M., Davies, A. M., Nery, E. D., Ebner, D., Montoya, M. C., Ostling, P., Pietiainen, V., Price, L. S., et al. (2016). Screening out irrelevant cell-based models of disease. Nat Rev Drug Discov.

Hoshi, K., Fujihara, Y., Mori, Y., Asawa, Y., Kanazawa, S., Nishizawa, S., Misawa, M., Numano, T., Inoue, H., Sakamoto, T., et al. (2016). Production of three-dimensional tissue-engineered cartilage through mutual fusion of chondrocyte pellets. Int J Oral Maxillofac Surg 45, 1177-1185.

Huang, M., Li, T., Pan, T., Zhao, N., Yao, Y., Zhai, Z., Zhou, J., Du, C., and Wang, Y. (2016). Controlling the strontium-doping in calcium phosphate microcapsules through yeast-regulated biomimetic mineralization. Regen Biomater 3, 269-276.

Irvine, S. A., and Venkatraman, S. S. (2016). Bioprinting and Differentiation of Stem Cells. Molecules 21.

Ishiguro, S., Cai, S., Uppalapati, D., Turner, K., Zhang, T., Forrest, W. C., Forrest, M. L., and Tamura, M. (2016). Intratracheal Administration of Hyaluronan-Cisplatin Conjugate Nanoparticles Significantly Attenuates Lung Cancer Growth in Mice. Pharm Res 33, 2517-2529.

Ivanov, D. P., Coyle, B., Walker, D. A., and Grabowska, A. M. (2016). In vitro models of medulloblastoma: Choosing the right tool for the job. J Biotechnol 236, 10-25.

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